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Amphibia: Anura: Leptodactylidae) Smithsonian Institution Scholarly Press smithsonian contributions to zoology • number 635 Smithsonian Institution Scholarly Press Variation,A Chronology Systematics, of and MiddleRelationships Missouri of Plainsthe Leptodactylus bolivianus ComplexVillage (Amphibia: Sites Anura: Leptodactylidae) By Craig M. Johnson W. Ronaldwith Heyer contributions and Rafael by O. de Sá Stanley A. Ahler, Herbert Haas, and Georges Bonani SERIES PUBLICATIONS OF THE SMITHSONIAN INSTITUTION Emphasis upon publication as a means of “diffusing knowledge” was expressed by the first Secretary of the Smithsonian. In his formal plan for the Institution, Joseph Henry outlined a program that included the following statement: “It is proposed to publish a series of reports, giving an account of the new discoveries in science, and of the changes made from year to year in all branches of knowledge.” This theme of basic research has been adhered to through the years by thousands of titles issued in series publications under the Smithsonian imprint, com- mencing with Smithsonian Contributions to Knowledge in 1848 and continuing with the following active series: Smithsonian Contributions to Anthropology Smithsonian Contributions to Botany Smithsonian Contributions to History and Technology Smithsonian Contributions to the Marine Sciences Smithsonian Contributions to Museum Conservation Smithsonian Contributions to Paleobiology Smithsonian Contributions to Zoology In these series, the Institution publishes small papers and full-scale monographs that report on the research and collections of its various museums and bureaus. The Smithsonian Contributions Series are distributed via mailing lists to libraries, universities, and similar institu- tions throughout the world. Manuscripts submitted for series publication are received by the Smithsonian Institution Scholarly Press from authors with direct affilia- tion with the various Smithsonian museums or bureaus and are subject to peer review and review for compliance with manuscript preparation guidelines. General requirements for manuscript preparation are on the inside back cover of printed volumes. For detailed submissions require- ments and to review the “Manuscript Preparation and Style Guide for Authors,” visit the Submissions page at www.scholarlypress.si.edu. smithsonian contributions to zoology • number 635 Variation, Systematics, and Relationships of the Leptodactylus bolivianus Complex (Amphibia: Anura: Leptodactylidae) W. Ronald Heyer and Rafael O. de Sá WASHINGTON D.C. 2011 ABSTRACT Heyer, W. Ronald, and Rafael O. de Sá. Variation, Systematics, and Relationships of the Lepto- dactylus bolivianus Complex (Amphibia: Anura: Leptodactylidae). Smithsonian Contributions to Zoology, number 635, viii + 58 pages, 21 figures, 20 tables, 2011.—The Leptodactylus bolivianus complex has been considered to consist of one or two species, L. bolivianus alone or L. bolivianus and L. insularum. Detailed morphological analyses were undertaken to evaluate variation in the complex, which ranges from Costa Rica through Panama, across northern South America in the river valleys draining to the Caribbean, and throughout much of the Amazon basin with southern limits in Bolivia. Members of the complex also occur on several islands off Nicaragua, Panama, and Colombia. Analyses of morphological and advertisement call data indicate that there are either two or three species comprising the complex. Analysis of molecular data strongly supports recognition of three species, one of which is described as a new species, Leptodactylus guianensis. The three species comprising the L. bolivianus clade are most closely related to the L. ocellatus clade within the genus Leptodactylus. Cover photos, from left to right: Leptodactylus insularum (Figure 17, courtesy of R. W. Mc- Diarmid), L. guianensis (Figure 15, courtesy of M. S. Hoogmoed), and L. bolivianus (Figure 12, courtesy of R. B. Cocroft). Published by SMITHSONIAN INSTITUTION SCHOLARLY PRESS P.O. Box 37012, MRC 957 Washington, D.C. 20013-7012 www.scholarlypress.si.edu Text and images in this publication may be protected by copyright and other restrictions or owned by indi- viduals and entities other than, and in addition to, the Smithsonian Institution. Fair use of copyrighted mate- rial includes the use of protected materials for personal, educational, or noncommercial purposes. Users must cite author and source of content, must not alter or modify content, and must comply with all other terms or restrictions that may be applicable. Users are responsible for securing permission from a rights holder for any other use. Library of Congress Cataloging-in-Publication Data Heyer, W. Ronald. Variation, systematics, and relationships of the Leptodactylus bolivianus complex (Amphibia: Anura: Leptodactylidae) / W. Ronald Heyer and Rafael O. de Sá. p. cm. — (Smithsonian contributions to zoology ; number 635) Includes bibliographical references. 1. Leptodactylus bolivianus—Classification. 2. Leptodactylus bolivianus—Variation. I. De Sá, Rafael O. II. Title. QL668.E257H49 2011 597.8’75—dc22 2011004864 ISSN: 0081-0282 (print); 1943-6696 (online) The paper used in this publication meets the minimum requirements of the American National Standard for Permanence of Paper for Printed Library Materials Z39.48–1992. Contents LIST OF FIGURES v LIST OF TABLES vii INTRODUCTION 1 METHODS AND MATERIALS 1 Juvenile and Adult Morphological Data 2 Larval Morphology 3 Advertisement Calls 4 Molecular Sequence Data 5 MEASUREMENT DATA 5 INTRASAMPLE VARIATION 6 Dorsal Pattern 8 Subocular Spot 9 Lip Stripe 9 Belly Pattern 9 Thigh Pattern 9 Shank Pattern 9 Dorsolateral Folds and Lateral Folds 9 Male Secondary Sexual Characters 9 Measurement Data 9 INTERSAMPLE VARIATION 12 Patterns and Folds 12 Dorsal Pattern 12 Subocular Spot 14 Lip Stripe 17 Belly Pattern 19 Thigh Pattern 19 Shank Pattern 20 Dorsolateral Folds 21 Lateral Folds 21 iv • SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY Male Secondary Sexual Characters 21 Measurement Data 22 GEOGRAPHIC VARIATION AMONG THE SAMPLES 23 Adult Form Morphological Characters 23 Larval Morphology 24 Advertisement Calls 25 Costa Rica Recording 25 Panama Recording 25 Peru Recording 25 MOLECULAR RELATIONSHIPS 26 INTERSPECIFIC VARIATION 27 Measurement Data 28 Morphological Data 29 Leptodactylus bolivianus and L. insularum Comparisons 30 Leptodactylus bolivianus: New Species Comparisons 30 Leptodactylus insularum: New Species Comparisons 30 SPECIES ACCOUNTS 30 Leptodactylus bolivianus Boulenger, 1898 31 Leptodactylus guianensis, new species 35 Leptodactylus insularum Barbour, 1906 38 ACKNOWLEDGMENTS 45 APPENDIX 1: OBSERVER ERROR ASSESSMENT FOR MORPHOLOGICAL DATA 47 APPENDIX 2: MOLECULAR SAMPLE LOCALITY DATA 55 REFERENCES 57 Figures 1. Locations of specimens used for intrasample analyses 7 2. Locations of 20 regional samples 17 3. Variation in posterior thigh patterns among 20 regional samples 20 4. Female discriminant function analysis results of 20 geographic samples 23 5. Levels of differentiation between geographically adjacent samples 23 6. Advertisement call of Leptodactylus from Costa Rica 26 7. Advertisement call of Leptodactylus from Panama 27 8. Advertisement call of Leptodactylus from Peru 28 9. Maximum likelihood cladogram of the Leptodactylus ocellatus species group 29 10. Plot of first two canonical vectors for male measurement data 29 11. Plot of first two canonical vectors for female measurement data 30 12. Leptodactylus bolivianus from Tambopata, Peru 32 13. Male thumb spines 32 14. Distributions of Leptodactylus bolivianus, L. guianensis, and L. insularum 34 15. Leptodactylus guianensis from northern Pará, Brazil 35 16. Lateral view of head, dorsal and ventral views of Leptodactylus guianensis, new species 36 17. Leptodactylus insularum from San Andrés, Colombia 38 18. Dorsal and ventral views of the lectotype of Leptodactylus insularum 39 19. Lateral view of Leptodactylus insularum tadpole 40 20. Oral disk of Leptodactylus insularum tadpole 40 Appendix 1 Figure A1.1. Example of design pattern 50 Tables 1. Statistics to determine observer error 6 2. Dorsal pattern state occurrences within Lower Río Chucunaque sample 8 3. Dorsal pattern state occurrences by age and sex within Lower Río Chucunaque sample 8 4. Chi-square occurrence values for character states of the dorsal pattern within Lower Río Chucunaque sample 8 5. Age and sex intrasample analyses results for dorsal pattern 8 6. Dorsal pattern, suborbital spot, lip pattern, and belly pattern state occurrences 10 7. Age and sex intrasample analyses results for subocular spot 11 8. Age and sex intrasample analyses results for lip stripe pattern 11 9. Age and sex intrasample analyses results for belly pattern 12 10. Age and sex intrasample analyses results for thigh pattern 12 11. Thigh pattern, shank pattern, dorsolateral fold, and lateral fold occurrences 13 12. Age and sex intrasample analyses results for dorsolateral folds 14 13. Age and sex intrasample analyses results for lateral folds 14 14. Male secondary sexual character state occurrences 15 15. Intrasample variation in measurement data 16 16. Intersample comparisons for dorsal pattern data 18 17. Number of males exhibiting secondary sexual character states 22 18. Quantitative larval data 24 19. Advertisement call data 25 20. Morphological character states for species pairs of the Leptodactylus bolivianus complex 31 Variation, Systematics, and Relationships of the Leptodactylus bolivianus Complex (Amphibia: Anura: Leptodactylidae) INTRODUCTION A cluster of morphologically
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